Evidence is compiled to demonstrate a redox scale within Earth's photosynthesisers that correlates the specificity of their RuBisCO with organismal metabolic tolerance to anoxia, and ecological selection by dissolved O 2/CO 2 and nutrients. The Form 1B RuBisCO found in the chlorophyte green algae, has a poor selectivity between the two dissolved substrates, O 2 and CO 2, at the active site. This enzyme appears adapted to lower O 2/CO 2 ratios, or more “anoxic” conditions and therefore requires additional energetic or nutrient investment in a carbon concentrating mechanism (CCM) to boost the intracellular CO 2/O 2 ratio and maintain competitive carboxylation rates under increasingly high O 2/CO 2 conditions in the environment. By contrast the coccolithophores and diatoms evolved containing the more selective Rhodophyte Form 1D RuBisCO, better adapted to a higher O 2/CO 2 ratio, or more oxic conditions. This Form 1D RuBisCO requires lesser energetic or nutrient investment in a CCM to attain high carboxylation rates under environmentally high O 2/CO 2 ratios. Such a physiological relationship may underpin the succession of phytoplankton in the Phanerozoic oceans: the coccolithophores and diatoms took over the oceanic realm from the incumbent cyanobacteria and green algae when the upper ocean became persistently oxygenated, alkaline and more oligotrophic. The facultatively anaerobic green algae, able to tolerate the anoxic conditions of the water column and a periodically inundated soil, were better poised to adapt to the fluctuating anoxia associated with periods of submergence and emergence and transition onto the land. The induction of a CCM may exert a natural limit to the improvement of RuBisCO efficiency over Earth history. Rubisco specificity appears to adapt on the timescale of ∼100 Myrs. So persistent elevation of CO 2/O 2 ratios in the intracellular environment around the enzyme, may induce a relaxation in RuBisCO selectivity for CO 2 relative to O 2. The most efficient RuBisCO for net carboxylation is likely to be found in CCM-lacking algae that have been exposed to hyperoxic conditions for at least 100 Myrs, such as intertidal brown seaweeds.
Dissolved O 2/CO 2 selects for a redox scale of phytoplankton Rubisco substrate selectivity and anaerobic metabolic ability.
Increasing O 2/CO 2 induced a positive feedback selecting for red-algal derived plastids at the start of the Mesozoic.
The relative affinity of RuBisCO for O 2 and CO 2 tunes to compensate for environmental O 2/CO 2 on timescales of 100–1000 yrs.
Induction of a CCM relaxes enzyme specificity over ∼ 100 Myrs providing a limit to improvement of RuBisCO selectivity.
Persistently high O 2/CO 2 ratios in restricted intertidal zones selects the most efficient RuBisCO in species lacking a CCM.